The goal of the present study was to establish the behavioral role of the nucleus accumbens (Nacc) core in the feed-forward spiraling striato-nigro-striatal circuitry that transmits information from the Nacc shell toward the dorsal subregion of the neostriatum (DS) in freely moving rats. Unilateral injection of μ-opioid receptor agonist [D-Ala(2),N-Me-Phe(4),Gly(5)-ol]-enkephalin (DAMGO; 1 and 2 μg), but not the δ 1-opioid receptor agonist [D-Pen(2,5)]-enkephalin (4 μg) or the δ2-opioid receptor agonist [D-Ala(2),Glu(4)]-deltorphin (2 μg), into the ventral tegmental area (VTA) produced contraversive circling in a dose-dependent manner. The effect of DAMGO was μ-opioid receptor-specific, because the μ-opioid receptor antagonist D-Phe-Cys-Tyr-D-Trp-Orn-Thr-Phe-Thr-NH2 (0.1 and 1 μg), which alone did not elicit any turning behavior, dose-dependently inhibited the effect of DAMGO. Injection of the dopamine D1/D2 receptor antagonist cis-(Z)-flupentixol (1 and 10 μg) into the Nacc shell ipsilaterally to the VTA significantly inhibited DAMGO (2 μg)-induced circling. Similar injections of cis-(Z)-flupentixol into the Nacc core inhibited DAMGO-induced circling, but, in addition, replaced circling by pivoting, namely turning behavior during which the rat rotates around its disfunctioning hindlimb. The present findings show that unilateral stimulation of μ-, but not δ-, opioid receptors in the VTA elicits contraversive circling that requires a relatively hyperdopaminergic activity in both the shell and the core of the Nacc at the opioid-stimulated side of the brain. The Nacc core plays an essential role in the transmission of information directing the display of pivoting that is elicited by an increased dopaminergic activity in the Nacc shell. It is concluded that the Nacc core is an essential link in the feed-forward spiraling striato-nigro-striatal circuitry that transmits information from the Nacc shell toward the DS in freely moving rats.